Litter Sex Ratio Research Articles

Early experiences modulate stress coping in a population of German shepherd dogs

Early experiences may alter later behavioural expressions in animals and these differences can be consistent through adulthood. In dogs, this may have a profound impact on welfare and working ability and, it is therefore interesting to evaluate how experiences during the first weeks of life contribute to shaping the long-term behaviour. We analysed data from 503 dogs from 105 litters, bred at the Swedish Armed Forces Dog Kennel. For each dog, the data comprised information on dam and sire, sex, litter size, sex ratio of litter, date of birth, and weight at birth, and at 10 days of age. Between the ages of 377 and 593 days, the dogs were tested in a temperament test, assessing their suitability as working dogs. The behaviour test comprised 12 different sub-tests, and was scored on a behavioural rating scale. A principal component analysis showed that the test performance could largely be attributed to four principal components (explaining 55.7% of variation), labelled Confidence, Physical Engagement, Social Engagement and Aggression. We analysed the effects of the different early life variables and sex on the principal component scores (PC scores) using linear modelling. PC scores on Confidence were affected by parity, sex and litter size, and Physical Engagement was affected by parity, growth rate, litter size and season of birth. Social Engagement was affected by growth rate and sex, and Aggression was affected by sex. Some of these effects disappeared when they were combined into a single linear model, but most of them remained significant also when controlling for collinearity. The results suggest that the early environment of dogs have long-lasting effects on their behaviour and coping styles in a stressful test situation and this knowledge can be used in the work with breeding of future military or police working dogs.

Competitive ability in male house mice (Mus musculus): genetic influences.

Conspecifics of many animal species physically compete to gain reproductive resources and thus fitness. Despite the importance of competitive ability across the animal kingdom, specific traits that influence or underpin competitive ability are poorly characterized. Here, we investigate whether there are genetic influences on competitive ability within male house mice. Additionally, we examined if litter demographics (litter size and litter sex ratio) influence competitive ability. We phenotyped two generations for a male's ability to possess a reproductive resource--a prime nesting site--using semi-natural enclosures with mixed sex groupings. We used the "Animal Model" coupled with an extensive pedigree to estimate several genetic parameters. Competitive ability was found to be highly heritable, but only displayed a moderate genetic correlation to body mass. Interestingly, litter sex ratio had a weak negative influence on competitive ability. Litter size had no significant influence on competitive ability. Our study also highlights how much remains unknown about the proximal causes of competitive ability.

The effect of cross breeding and reciprocal crossing on the reproductive performance of rabbits in Minna, Nigeria

The effect of Cross breeding and reciprocal crossing on birth, weaning and growth traits of two strains [Chinchilla (CH) and New Zealand white (NZW)] of rabbits aged between 3-4 months were investigated. A total of eighteen (18) does (nine does per strain) and six (6) bucks (three bucks per strain) were used in this study. Three (3) does per strain were assigned to a buck from the opposite strain for mating and the treatment was replicated. The does were mated when they attained the age of 5 months. Birth traits like litter size, litter weight, gestation length, gestation gain, kindling loss and neo-natal mortality were observed. At weaning, litter size, litter weight, litter weight gain, sex ratio and survival rate were monitored. Growth traits like body weight, nose to shoulder length, shoulder to tail length, trunk, ear length and heart girths were monitored at 21, 35 and 49 days. Results obtained showed that Chinchilla (CH) buck crossed with New Zealand white (NZW) does produced offspring with significantly (P< 0.05) better body weight, nose to shoulder length, shoulder to tail length, heart girth, trunk and kindling loss. However, results obtained for neo-natal mortality was better in the offspring from NZW bucks and CH does. It was concluded that progenies from the crosses between CH bucks and NZW does, were better than progenies from the crosses between NZW bucks and CH does.

Calcium availability influences litter size and sex ratio in white-footed mice (Peromyscus leucopus).

The production of offspring typically requires investment of resources derived from both the environment and maternal somatic reserves. As such, the availability of either of these types of resources has the potential to limit the degree to which resources are allocated to reproduction. Theory and empirical studies have argued that mothers modify reproductive performance relative to exogenous resource availability and maternal condition by adjusting size, number or sex of offspring produced. These relationships have classically been defined relative to availability of energy sources; however, in vertebrates, calcium also plays a critical role in offspring production, as a considerable amount of calcium is required to support the development of offspring skeleton(s). We tested whether the availability of calcium influences reproductive output by providing female white-footed mice with a low-calcium or standard diet from reproductive maturity to senescence. We then compared maternal skeletal condition and reproductive output, based on offspring mass, offspring number and litter sex ratio, between dietary treatments. Mothers on the low-calcium diet exhibited diminished skeletal condition at senescence and produced smaller and strongly female-biased litters. We show that skeletal condition and calcium intake can influence sex ratio and reproductive output following general theoretical models of resource partitioning during reproduction.

Is there an expected relationship between parental expenditure and sex ratio of litters or broods?

Parents may be selected to adjust the sex ratio of their offspring when parental expenditure yields different fitness returns from sons and daughters. This prediction is clear when parents produce only one offspring per reproductive attempt, but more complicated when parental resources are shared by several offspring, and parents may potentially influence the resource allocation among offspring as well as their number and sex. Here we present an optimization model to make predictions on how total parental expenditure may relate to the number and sex of offspring at every rank position within the litter or brood as well as the sex ratio of the litter/brood for the case of a large population with stable Fisherian sex ratio. We show that selection for sex ratio adjustment should be stronger for offspring at higher-ranking positions, for which the amount of resources received can be more predictable. Also, the relationship between parental resources devoted to a litter/brood of a given size and the primary sex ratio (proportion of males) is not expected to be a monotonically increasing function but rather a J-shaped relationship, steeper for small litters/broods and more extreme sexual dimorphism. Parental expenditure relates to increased sex ratio only for small variations in parental expenditure and for a given brood/litter size. For variable litter/brood sizes, a general relationship between parental resources and litter/brood sex ratio is not expected, although in practice pooling litters or broods of different sizes may produce negative relationships between parental expenditure and sex ratio of the litter/brood.

Litter reductions reveal a trade-off between offspring size and number in brown bears

Experimental manipulations have revealed positive effects of litter reduction on offspring mass in small mammals, but little is known about this trade-off in large mammals. We examined the determinants of natural litter size variation and quantified the effects of litter size, maternal characteristics, and litter composition on yearling mass using 24 years of data on marked brown bears (Ursus arctos) in Sweden. Infanticide by adult males is a major cause of cub-of-the-year mortality, leading to litter size reductions. Litter size (n = 265) at den emergence ranged from one to four cubs (average, 2.7) and increased with maternal age. Litter size, however, appeared independent of maternal size, population density, interlitter interval, study area, or previous litter sex ratio. Yearling body mass increased with maternal body size but was independent of litter sex ratio. Litter size and yearling mass were negatively correlated, mostly because singletons were about 30 % heavier than yearlings from litters of two to four cubs. In reduced litters, survivors were on average 8 % heavier as yearlings than individuals from intact litters, suggesting that sibling competition reduces growth. Trade-offs between litter size and yearling mass in bears appear similar in magnitude to those found in small mammals.

Effect of glucose concentration during in vitro culture of mouse embryos on development to blastocyst, success of embryo transfer, and litter sex ratio

A high-glucose concentration in the reproductive tract during early development may result in aberrant embryo or fetal development, with effects that could have a greater impact on one sex than the other. Here, we determine if a high-glucose concentration impacts embryo development and pregnancy outcomes in a sex-specific manner in the mouse. Zygotes were cultured in potassium simple optimized medium, which typically contains 0.2 mM D-glucose, with and without additional glucose supplementation to a concentration of 28 mM. Zygote cleavage and blastocyst rate did not differ between treatments, but total and trophectoderm cell counts were reduced in blastocysts cultured in a high glucose. No differences between sexes nor inner cell mass cell number were observed within each treatment. Blastocysts developed in both media were transferred to recipients. The percentage of blastocysts resulting in viable pups was significantly reduced when the blastocysts were cultured in 28 mM glucose (74 ± 4%, controls vs. 55.8 ± 7.1%, 28 mM glucose), but conceptus loss affected both sexes equally as litter sex ratio did not differ between treatments (52.7% and 52.2% males for controls and high glucose, respectively). Pup body weight at birth was higher for males than females, but was not affected by earlier culture in high glucose. In conclusion, in vitro culture in medium with a glucose concentration approximating that of diabetic serum reduces total and trophectoderm cell numbers at the blastocyst stage and conceptus development to term, but these detrimental effects are not sex-specific.

Secondary Sex Ratios in Six Snake Species

Sex ratios at birth or hatching in snake populations are often assumed to be 1∶1 in agreement with Fisherian theory. We evaluated secondary sex ratios (SSRs) in two viperids (Sistrurus catenatus and S. miliarius) and four natricine colubrids (Nerodia rhombifer, Thamnophis proximus, T. radix, and T. sirtalis). We captured 274 gravid females that produced 2443 living offspring. Population-level SSRs in our focal species did not differ significantly from 1∶1. In addition, variation in individual litter SSRs conformed to expectations generated by the binomial distribution with an even sex ratio. Each species showed individual variation in SSRs; however, the majority of variation in litter SSRs was not explained by variation in the maternal or litter characteristics we examined. The three exceptions were a very strong negative association between mean offspring mass and litter SSR in T. radix (r2 = 0.96), a strong positive association between mean offspring mass and litter sex ratio in T. proximus (r2 = 0.40), and a strong positive association between maternal condition and litter SSR in T. proximus (r2 = 0.40). Whether or not these relationships have functional or adaptive significance warrants further study. The majority of our results were unsurprising and not statistically significant. We suggest, however, that the presentation and publication of both non-significant and significant results is exactly what is needed to give an accurate view of SSRs at both the population level and the maternal level in snakes.

Litter sex ratio affects lifetime reproductive success of free‐living female Alpine marmots Marmota marmota†

ABSTRACTIn litter‐bearing mammals, adult phenotype is influenced during prenatal life by the sex of neighbouring foetuses. This phenomenon, found so far only in laboratory studies, may have ecological importance in nature. We present the first evidence that litter sex ratio has consequences for lifetime reproductive success in mammals. Female Alpine marmots born in a male‐biased litter, i.e. more likely to be located in utero next to male foetuses, are more likely to be dominant later in life – a prerequisite for reproduction in this species. We found no evidence for lower reproductive output of these females, a common cost of prenatal masculinization.

Stress-induced sex ratios in ground squirrels: support for a mechanistic hypothesis

Systematic deviations in sex ratio may be adaptive in the face of the prevailing environmental or physiological cues experienced by the mother; yet some theoretical and mechanistic hypotheses remain at odds and are rarely examined noninvasively under natural conditions. Conventional interpretations of the Trivers and Willard (Trivers RL, Willard DE. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science 179:90–92) hypothesis (TWH) predict that higher stress should be associated with female-biased litters; yet, several mechanistic hypotheses predict the opposite. We tested the predictions of the TWH and 2 stress-related mechanistic hypotheses in a free-living polygynandrous sciurid, Richardson’s ground squirrel, Urocitellus richardsonii. We examined the relationship between litter sex ratio and indicators of maternal condition and investment. These included litter size, juvenile mass at emergence, as well as maternal age, changes in maternal body mass, and maternal fecal glucocorticoid (cortisol and corticosterone) levels during gestation, lactation, and post-weaning. Males born of small litters were significantly heavier at emergence than males from larger litters, which were female biased, whereas females showed no significant change in mass with litter size. Mothers with higher fecal cortisol levels during the gestation period (but not during lactation or post-weaning) were more likely to produce male-biased litters, whereas females producing larger litters showed significantly higher cortisol levels during lactation (but not gestation or post-weaning) than mothers producing smaller litters. Our results provide support for both the proximate glucose-mediated mechanistic model of Cameron (Cameron EZ. 2004. Facultative adjustment of mammalian sex ratios in support of the Trivers-Willard hypothesis: evidence for a mechanism. Proc R Soc Ser B Biol Sci. 271:1723–1728) and the broad-sense TWH, where social and life-history characteristics play an integral role.

Does gestational temperature or prenatal sex ratio influence development of sexual dimorphism in a viviparous skink?

Prenatal sex ratio (through exposure to hormones from siblings in utero) can influence sexually dimorphic traits of many mammals; but research on viviparous reptiles has contrasting outcomes, which have yet to be resolved. The thermal environment experienced during gestation has a strong effect on the phenotype of reptiles, but whether this thermal effect overrides that of prenatal sex ratio has yet to be explored. We experimentally investigated whether the gestation temperature, or litter sex ratio, influences sexually dimorphic traits (head width and axilla-groin length) in a viviparous skink (Oligosoma maccanni). We found that gestation temperature had a significant influence on sexually dimorphic traits of neonates, and at 3 months of age still influenced head width. We found no evidence that traits in either sex were masculinized or feminized in response to litter sex ratio. The development of external sexual dimorphisms increased gradually (all thermal regimes pooled), with neonates showing no sexual dimorphism, 3-month-old juveniles showing some sexual dimorphism in head width, and adults having stronger, but incompletely separated, sexual dimorphism for both traits. We suggest that the overlap in sexually dimorphic traits of adult O. maccanni (and perhaps other reptiles) may be better explained by natural variation in temperatures experienced during embryonic development, rather than hormonal effects arising from litter sex ratio. The interaction of hormones and temperature during gestation and the effect of these factors on sexual dimorphism within reptiles deserve further exploration.

Restricted feed intake in lactating primiparous sows. II. Effects on subsequent litter sex ratio and embryonic gene expression

Expression of panels of candidate genes controlling myogenesis, angiogenesis and gender-specific imprinting of development were analysed in embryonic, placental and endometrial tissues recovered at Day 30 of gestation from a subset of primiparous sows that were either feed restricted (Restrict; n=17) or fed to appetite (Control; n=15) during the last week of the previous lactation. Embryos were also sex typed to investigate gender bias in response to treatments. Average embryonic weight was lower in the subset of Restrict compared with Control litters (1.38±0.07vs 1.59±0.08g, respectively) and the male:female sex ratio was higher (P<0.05) in embryos (litters) recovered from Restrict sows. Treatment affected (P≤0.05) the expression of embryonic and placental genes involved in insulin-like growth factor (IGF) 2 signalling, including IGF2, INSR and IGF2R. Embryonic expression of ESR1 was also affected by treatment (P<0.03) and sex×treatment interactions were observed for the expression of embryonic ESR1 (P<0.05) and placental ANGPT2 (P<0.03). At the molecular level, these results support the suggestion that changes in placental function are not the primary mechanism mediating detrimental effects of previous sow catabolism on early embryonic development in the feed-restricted lactational sow model. However, perturbations in the IGF2 system are implicated as mediators of these effects.

Nutritional Restriction Prior to Conception in the Sow Alters Embryonic Development and Candidate Gene Expression in the Placenta and Endometrium.

The extent to which maternal nutrition alters placental and fetal development through epigenetic mechanisms, is still uncertain. In an established experimental model using the catabolic primiparous sow, feed restriction during lactation affects embryonic survival and development during the subsequent gestation. In a continuation of these studies, primiparous sows (n=34) were either fully fed (Control:C) or restricted to 60% of voluntary feed intake (Restrict:R) during the third week of a 21-d lactation and re-bred after weaning. Sows were euthanized at d 30 of gestation and reproductive and litter characteristics were recorded. Embryos and placentae (n=488 of each) were collected for each sow, and a sample of endometrium (n=68) was taken from the left and right horn from each sow, frozen immediately in liquid nitrogen and stored at -80°C. Total RNA was extracted from placental, endometrial and embryonic samples collected, DNAse-treated, reverse transcribed, and real-time PCR was used to determine transcript abundance of candidate genes involved in regulating endometrial and placental vascularity and embryonic muscle development. The relative deltaCt values were calculated using cyclophilin as an internal control, and data were analyzed using mixed models analysis with treatment and sex of embryo as independent variables and sow as a random variable. There were no differences in ovulation rate, embryonic survival or number of embryos in utero between C and R sows. However, litter sex ratio was different with more males in the R sows (P<0.05) and embryo weight was reduced (P<0.05) in R compared to C sows. Embryo weight and litter sex ratio were also related to sow weight loss in the previous lactation. When genes regulating vascular development were considered, FGF2 and VEGFA mRNA expression was lower in the endometrium, while ANGPT2 was lower (P<0.05) in the placenta, recovered from R sows. Expression of myogenic regulatory factors analyzed (MYF5, MYF6, MYOG, MYOD1, PAX3, GLI1 and WNT10b) was not different between C and R sows at d 30 of gestation. In addition, the expression of some imprinted genes were examined, and IGF2 expression tended to be higher (P=0.059) and INSR expression was higher (P=0.049) in the R embryos, and IGF2R demonstrated a tendency for a sex by treatment interaction (P=0.066) in the placenta. These results confirm that maternal metabolic state prior to conception can adversely affect embryonic size and sex ratio in the next litter. These effects involved expression of genes related to vascular development in the uterus and placenta, and were consistent with the concept of epigenetic regulation of developmentally important genes. (platform)

Maternal gestational androgen levels in female marmosets ( Callithrix geoffroyi) vary across trimesters but do not vary with the sex ratio of litters

Maternal hormones can dramatically modify offspring phenotypes via organizational actions on morphological and behavioral development. In placental mammals, there is the possibility that some portion of hormones in maternal circulation may be derived from fetal origin. We tested the possibility that maternal androgens in pregnant female marmosets reflected, in part, contributions from male fetuses by comparing levels of urinary androgens across pregnancy in females carrying varying numbers of male offspring. We monitored urinary androgen excretion in 18 pregnancies from five female white-faced marmosets ( Callithrix geoffroyi). Androgen levels rose significantly in the first trimester of pregnancy, reached a peak in the middle of the second trimester, and then declined gradually until parturition. At no point in pregnancy were levels of urinary androgens higher in females carrying litters that had 50% or more males than in females carrying litters that were less than 50% male. Levels of maternal androgens were not associated with litter size, the number of males in the litter, or with the proportion of the litter that was male. The high levels of androgen in pregnant females are therefore likely of strictly maternal origin, and any modification of fetal growth and development can be considered a ‘maternal effect’.

Comparison of life‐history characteristics of island and mainland populations of the swamp antechinus

AbstractThe reproductive ecology of the swamp antechinus Antechinus minimus, a small dasyurid (Dasyuridae) marsupial with obligate male semelparity, was investigated in populations inhabiting the mainland coast and on a nearby offshore island in south‐eastern Australia. The size and sex ratios of litters, individual body mass and size, timing of births and female longevity were determined from live‐trapped animals. The island population had significantly smaller litter sizes and greater adult body mass in comparison with the mainland population. This is consistent with features of the ‘island syndrome’, which predicts directional selection for these traits in high‐density populations with reduced extrinsic mortality. However, inter‐annual variability in litter sizes in the island population suggests that litter size is more responsive to fluctuating local conditions, such as population density, which is likely to affect food availability, rather than directional genetic changes. In contrast with other antechinus species, biased sex ratios were not evident. In addition, large variations of the timing of births were estimated at both sites and these appear to be related to seasonal conditions such as autumn rainfall and female body mass before mating.

An unstable social environment affects sex ratio in guinea pigs: an adaptive maternal effect?

AbstractEvolutionary theory suggests that offspring sex should be adjusted to environmental conditions in order to maximize future reproductive success. In several animal taxa environmental factors indeed affect the secondary sex ratio. In humans, changes in the sex ratio at birth have been associated with population stressors like war, environmental disasters or economic strife during pregnancy. Here we compared litter sex ratios of female guinea pigs, exposed experimentally to a stable and an unstable social environment. In the latter group composition was changed every three days. Under unstable social conditions the sex ratio was significantly more biased towards daughters than in the stable social situation. This finding was consistent among four independent experiments, conducted independently from each other. Life expectancy can be dramatically reduced under conditions of social instability. Hence mothers in such conditions should bias their investment towards the sex that reaches sexual maturity first, which is the female sex in this species. Thus, to shift the offspring sex ratio towards more daughters under conditions of social instability may represent a maternal strategy to maximize future reproductive success.

Uterine Crowding in the Sow Affects Litter Sex Ratio, Placental Development, and Embryonic Myogenin mRNA Expression in Early Gestation.

Uterine Crowding in the Sow Affects Litter Sex Ratio, Placental Development, and Embryonic Myogenin mRNA Expression in Early Gestation.

Effects of Perinatal Polychlorinated Biphenyls on Adult Female Rat Reproduction: Development, Reproductive Physiology, and Second Generational Effects1

Perinatal exposures to endocrine-disrupting chemicals, such as polychlorinated biphenyls (PCBs), can cause latent effects on reproductive function. Here, we tested whether PCBs administered during late pregnancy would compromise reproductive physiology in both the fetally exposed female offspring (F1 generation), as well as in their female offspring (F2 generation). Pregnant Sprague-Dawley rats were treated with the PCB mixture, Aroclor 1221 (A1221; 0, 0.1, 1, or 10 mg/kg), on Embryonic Days 16 and 18. Somatic and reproductive development of F1 and their F2 female offspring were monitored, including ages of eye opening, pubertal landmarks, and serum reproductive hormones. The results showed that low doses of A1221 given during this critical period of neuroendocrine development caused differential effects of A1221 on F1 and F2 female rats. In both generations, litter sex ratio was skewed toward females. In the F1 generation, additional effects were found, including a significant alteration of serum LH in the 1 mg/kg A1221 group. The F2 generation showed more profound alterations, particularly with respect to fluctuations in hormones and reproductive tract tissues across the estrous cycle. On proestrus, the day of the preovulatory GnRH/gonadotropin surge, F2 females whose mothers had been exposed perinatally to A1221 exhibited substantially suppressed LH and progesterone concentrations, and correspondingly smaller uterine and ovarian weights on estrus, compared with F2 descendants of control rats. These latter changes suggest a dysregulation of reproductive physiology. Thus, low levels of exposure to PCBs during late fetal development cause significant effects on the maturation and physiology of two generations of female offspring. These findings have implications for reproductive health and fertility of wildlife and humans.

Generation of sex ratio biases in the red-tailed phascogale (Phascogale calura)

Male semelparous dasyurid species are annual breeders that use a promiscuous mating system. These species have shown biases in litter sex ratios and, with females producing more young than they have available teats, this provides an opportunity for the manipulation of the sex ratio at birth. The sex ratio of embryos and pouch young, and the degree of embryonic overproduction, in red-tailed phascogales (Phascogale calura) was investigated to gain an understanding of the mechanism by which sex biases may be generated. The sex ratio of embryos did not differ from parity, but a male bias was observed in young attaching to teats. Females produced an average of 15.1 +/- 1.9 corpora lutea and 10.5 +/- 3.5 viable embryos, with no difference in fecundity observed with female age or weight. Because females only have eight teats, the overproduction of young, and male-biased attachment, was sufficient to explain the observed male bias in pouch young. No relationship was observed between maternal weight and sex ratio, but heavier females did tend to produce more ova. Meta-analysis of studies providing information on litter sex ratios in male semelparous dasyurid species did not show any consistent trend.

Uterine crowding in the sow affects litter sex ratio, placental development and embryonic myogenin expression in early gestation

Uterine crowding in the pig results in intrauterine growth restriction (IUGR), and permanently affects fetal muscle fibre development, representing production losses for the commercial pig herd. The present study sought to understand how different levels of uterine crowding in sows affects muscle fibre development in the early embryo at the time of muscle fibre differentiation and proliferation. Sows either underwent surgical, unilateral oviduct ligation (LIG; n = 10) to reduce the number of embryos in the uterus, or remained as intact, relatively-crowded controls (CTR; n = 10). Embryos and placentae were collected at Day 30 of gestation, and myogenic regulatory factor (MRF) transcript abundance was determined using real-time PCR for both myogenin (MYOG) and myoblast differentiation 1 (MYOD1). Unilateral tubal ligation resulted in lower numbers of embryos in utero, higher placental weights and a higher male : female sex ratio (P < 0.05). Relative MYOD1 expression was not different, but MYOG expression was higher (P < 0.05) in the LIG group embryos; predominantly due to effects on the male embryos. Relatively modest uterine crowding therefore affects MRF expression, even at very early stages of embryonic development, and could contribute to reported differences in fetal muscle fibre development, birthweight and thus post-natal growth performance in swine.